Interkingdom Detection of Bacterial Quorum-Sensing Molecules by Mammalian Taste Receptors

Abstract

Bitter and sweet taste G protein-coupled receptors (known as T2Rs and T1Rs, respectively) were originally identified in type II taste cells on the tongue, where they signal perception of bitter and sweet tastes, respectively. Over the past ~15 years, taste receptors have been identified in cells all over the body, demonstrating a more general chemosensory role beyond taste. Bitter and sweet taste receptors regulate gut epithelial function, pancreatic β cell secretion, thyroid hormone secretion, adipocyte function, and many other processes. Emerging data from a variety of tissues suggest that taste receptors are also used by mammalian cells to “eavesdrop” on bacterial communications. These receptors are activated by several quorum-sensing molecules, including acyl-homoserine lactones and quinolones from Gram-negative bacteria such as Pseudomonas aeruginosa, competence stimulating peptides from Streptococcus mutans, and D-amino acids from Staphylococcus aureus. Taste receptors are an arm of immune surveillance similar to Toll-like receptors and other pattern recognition receptors. Because they are activated by quorum-sensing molecules, taste receptors report information about microbial population density based on the chemical composition of the extracellular environment. This review summarizes current knowledge of bacterial activation of taste receptors and identifies important questions remaining in this field.

Tastant-receptor interactions: insights from the fruit fly

“…Unexpectedly, this receptor uses nuclear factor-κB ( NF -κB)/immune deficiency (IMD)-dependent signaling to activate “bitter” GRNs ( 60 ). An interest in the role of oral taste receptors in microbial detection has emerged in mammalian research ( 78 , 79 ), and this recent work in fruit flies highlights an unexpected role for NF -κB/IMD signaling in taste cells that impacts feeding choices ( 60 ).…”

Remodeling of Paranasal Sinuses Mucosa Functions in Response to Biofilm-Induced Inflammation

“…20,67 Moreover, due to recognition by T2Rs bacterial quorum sensing molecules (QSMs), eg, 3-oxo-C12-HSL (C12-HSL), T2Rs provide information about the population density of microorganisms based on the chemical composition of the extracellular environment. 120 In addition, T2Rs may mediate tumor-microbiome crosstalk via T2R-driven apoptotic pathways. 120 Overall, T2Rs activation led to enhanced bacteria phagocytosis by airway ciliated cells through T2R-eNOS pathway and control AMP secretion.…”

“…120 In addition, T2Rs may mediate tumor-microbiome crosstalk via T2R-driven apoptotic pathways. 120 Overall, T2Rs activation led to enhanced bacteria phagocytosis by airway ciliated cells through T2R-eNOS pathway and control AMP secretion. For instance, activation of T2R38 by P. aeruginosa C12-HSL results in a signaling cascade with resultant Ca 2+ -dependent release of bactericidal nitric oxide and increased ciliary beat frequency.…”

“…122 Hence, T2Rs may play a pivotal role in microbial surveillance and host-bacteria interactions that may be augmented by T2Rs gene polymorphisms, eg, altering T2Rs response to sugars and, in turn, T2R-mediated AMP secretion. 30,120,123 For example, in CRS patients, glucose concentration in nasal secretions is 3-to 4-fold higher than in healthy individuals, resulting in lower AMP levels. 121 In contrast, activation of FPRs (FPR-1, FPR-2, and FPR-) by N-formylated peptides present in bacterial cells or S. aureus superantigen-like (SSL) toxin 13 (SSL13) is associated with increased release of molecules responsible for tissue remodeling by epithelial cells, such as VEGF-A, TGF-β, and MMPs (MMP-2, MMP-7, and MMP-9), parallel to the reduced expression of tissue inhibitors of MMPs (TIMP-1 and TIMP-2), indicating their role in nasal polyp formation (Figure 3).…”

The taste for health: the role of taste receptors and their ligands in the complex food/health relationship

“…The involvement of taste in this scenario has been, for a long time, limited to its participation in the control of motivational processes that guide eating behavior and food choices, allowing the recognition of nutrients, while avoiding potential toxic compounds (5,6). The identification of taste receptors, particularly the G protein-coupled receptors (GPCRs) that mediate sweet, umami, and bitter tastes, in the gastrointestinal (GI) tract [as well as in many other locations, not the subject of this article, (7)] has revealed many more relevant tasks for them, from nutrient sensing and consequent hormone release to microbiota composition and immune response (8)(9)(10).…”